Recent evidence of non-systemic transmission of West Nile virus in mosquitoes has stimulated interest in the consequences for the epidemiology of arboviruses. This alternative route of transmission may affect arbovirus epidemiology in several ways. For example, a virus may spread through a host community more quickly if non-systemic transmission occurs, since there is no latent period in the host. Non-systemic transmission expands the range of vertebrate hosts which support mosquito infection; we currently do not know which vertebrates facilitate non-systemic transmission. We use simple mathematical models to extend previous work comparing non-systemic and viremic (conventional) transmission modes. The relative importance of the two modes of transmission depends on their relative efficiencies and host availability. Aggregation of vectors on individual hosts is important, but is moderated by longer periods of transmission and transmission over broader spatial distributions. The models highlight areas where further data are needed, such as the efficiency of non-systemic transmission at different spatial and temporal scales. As these scales of non-systemic transmission increase, the transmission potential becomes similar to viremic transmission on hosts with low viremia. In combination with previous studies on non-viremic transmission and the importance of hosts with low viremias, these models demonstrate that we must re-evaluate many conventional beliefs about arbovirus transmission and consider a broader range of potential transmission opportunities. It is likely, however, that alternative modes of transmission or low viremia hosts will be of more importance in the early stages of virus transmission and less important during major outbreaks.